Mechanical forces inducing oxaliplatin resistance in pancreatic cancer can be targeted by autophagy inhibition

Abstract Pancreatic cancer remains one of the most lethal malignancies, with limited treatment options and poor prognosis. A common characteristic among pancreatic cancer patients is the biomechanically altered tumor microenvironment (TME), which among others is responsible for the elevated mechanic...

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Main Authors: Maria Kalli, Fotios Mpekris, Antonia Charalambous, Christina Michael, Chrystalla Stylianou, Chrysovalantis Voutouri, Andreas G. Hadjigeorgiou, Antonia Papoui, John D. Martin, Triantafyllos Stylianopoulos
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-07268-1
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author Maria Kalli
Fotios Mpekris
Antonia Charalambous
Christina Michael
Chrystalla Stylianou
Chrysovalantis Voutouri
Andreas G. Hadjigeorgiou
Antonia Papoui
John D. Martin
Triantafyllos Stylianopoulos
author_facet Maria Kalli
Fotios Mpekris
Antonia Charalambous
Christina Michael
Chrystalla Stylianou
Chrysovalantis Voutouri
Andreas G. Hadjigeorgiou
Antonia Papoui
John D. Martin
Triantafyllos Stylianopoulos
author_sort Maria Kalli
collection DOAJ
description Abstract Pancreatic cancer remains one of the most lethal malignancies, with limited treatment options and poor prognosis. A common characteristic among pancreatic cancer patients is the biomechanically altered tumor microenvironment (TME), which among others is responsible for the elevated mechanical stresses in the tumor interior. Although significant research has elucidated the effect of mechanical stress on cancer cell proliferation and migration, it has not yet been investigated how it could affect cancer cell drug sensitivity. Here, we demonstrated that mechanical stress triggers autophagy activation, correlated with increased resistance to oxaliplatin treatment in pancreatic cancer cells. Our results demonstrate that inhibition of autophagy using hydroxychloroquine (HCQ) enhanced the oxaliplatin-induced apoptotic cell death in pancreatic cancer cells exposed to mechanical stress. The combined treatment of HCQ with losartan, a known modulator of mechanical abnormalities in tumors, synergistically enhanced the therapeutic efficacy of oxaliplatin in murine pancreatic tumor models. Furthermore, our study revealed that the use of HCQ enhanced the efficacy of losartan to alleviate mechanical stress levels and restore blood vessel integrity beyond its role in autophagy modulation. These findings underscore the potential of co-targeting mechanical stresses and autophagy as a promising therapeutic strategy to overcome drug resistance and increase chemotherapy efficacy.
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spelling doaj-art-e3d015c1de334d268b1e8278dbb4f49e2025-08-20T02:51:18ZengNature PortfolioCommunications Biology2399-36422024-11-017111710.1038/s42003-024-07268-1Mechanical forces inducing oxaliplatin resistance in pancreatic cancer can be targeted by autophagy inhibitionMaria Kalli0Fotios Mpekris1Antonia Charalambous2Christina Michael3Chrystalla Stylianou4Chrysovalantis Voutouri5Andreas G. Hadjigeorgiou6Antonia Papoui7John D. Martin8Triantafyllos Stylianopoulos9Cancer Biophysics Laboratory, Department of Mechanical and Manufacturing Engineering, University of CyprusCancer Biophysics Laboratory, Department of Mechanical and Manufacturing Engineering, University of CyprusCancer Biophysics Laboratory, Department of Mechanical and Manufacturing Engineering, University of CyprusCancer Biophysics Laboratory, Department of Mechanical and Manufacturing Engineering, University of CyprusCancer Biophysics Laboratory, Department of Mechanical and Manufacturing Engineering, University of CyprusCancer Biophysics Laboratory, Department of Mechanical and Manufacturing Engineering, University of CyprusCancer Biophysics Laboratory, Department of Mechanical and Manufacturing Engineering, University of CyprusCancer Biophysics Laboratory, Department of Mechanical and Manufacturing Engineering, University of CyprusMateria TherapeuticsCancer Biophysics Laboratory, Department of Mechanical and Manufacturing Engineering, University of CyprusAbstract Pancreatic cancer remains one of the most lethal malignancies, with limited treatment options and poor prognosis. A common characteristic among pancreatic cancer patients is the biomechanically altered tumor microenvironment (TME), which among others is responsible for the elevated mechanical stresses in the tumor interior. Although significant research has elucidated the effect of mechanical stress on cancer cell proliferation and migration, it has not yet been investigated how it could affect cancer cell drug sensitivity. Here, we demonstrated that mechanical stress triggers autophagy activation, correlated with increased resistance to oxaliplatin treatment in pancreatic cancer cells. Our results demonstrate that inhibition of autophagy using hydroxychloroquine (HCQ) enhanced the oxaliplatin-induced apoptotic cell death in pancreatic cancer cells exposed to mechanical stress. The combined treatment of HCQ with losartan, a known modulator of mechanical abnormalities in tumors, synergistically enhanced the therapeutic efficacy of oxaliplatin in murine pancreatic tumor models. Furthermore, our study revealed that the use of HCQ enhanced the efficacy of losartan to alleviate mechanical stress levels and restore blood vessel integrity beyond its role in autophagy modulation. These findings underscore the potential of co-targeting mechanical stresses and autophagy as a promising therapeutic strategy to overcome drug resistance and increase chemotherapy efficacy.https://doi.org/10.1038/s42003-024-07268-1
spellingShingle Maria Kalli
Fotios Mpekris
Antonia Charalambous
Christina Michael
Chrystalla Stylianou
Chrysovalantis Voutouri
Andreas G. Hadjigeorgiou
Antonia Papoui
John D. Martin
Triantafyllos Stylianopoulos
Mechanical forces inducing oxaliplatin resistance in pancreatic cancer can be targeted by autophagy inhibition
Communications Biology
title Mechanical forces inducing oxaliplatin resistance in pancreatic cancer can be targeted by autophagy inhibition
title_full Mechanical forces inducing oxaliplatin resistance in pancreatic cancer can be targeted by autophagy inhibition
title_fullStr Mechanical forces inducing oxaliplatin resistance in pancreatic cancer can be targeted by autophagy inhibition
title_full_unstemmed Mechanical forces inducing oxaliplatin resistance in pancreatic cancer can be targeted by autophagy inhibition
title_short Mechanical forces inducing oxaliplatin resistance in pancreatic cancer can be targeted by autophagy inhibition
title_sort mechanical forces inducing oxaliplatin resistance in pancreatic cancer can be targeted by autophagy inhibition
url https://doi.org/10.1038/s42003-024-07268-1
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